ORIGINAL RESEARCH
published: 10 July 2018
Edited by:
Xiaolin Zhou,
Peking University, China
Reviewed by:
Gennady Knyazev,
State Scientific-Research Institute of
Physiology & Basic Medicine, Russia
Katharina Paul,
Ghent University, Belgium
*Correspondence:
Xuhai Chen
shiningocean@snnu.edu.cn
Received: 17 February 2018
Accepted: 13 June 2018
Published: 10 July 2018
Citation:
Chen X, Yuan H, Zheng T, Chang Y
and Luo Y (2018) Females Are More
Sensitive to Opponent’s Emotional
Feedback: Evidence From
Event-Related Potentials.
Front. Hum. Neurosci. 12:275.
doi: 10.3389/fnhum.2018.00275
Frontiers in Human Neuroscience | www.frontiersin.org
doi: 10.3389/fnhum.2018.00275
Females Are More Sensitive to
Opponent’s Emotional Feedback:
Evidence From Event-Related
Potentials
Xuhai Chen*, Hang Yuan , Tingting Zheng , Yingchao Chang and Yangmei Luo
Key Laboratory of Behavior and Cognitive Psychology in Shaanxi Province, School of Psychology, Shaanxi Normal University,
Xi’an, China
It is widely believed that females outperformed males in emotional information
processing. The present study tested whether the female superiority in emotional
information processing exists in a naturalistic social-emotional context, if so, what
the temporal dynamics underlies. The behavioral and electrophysiological responses
were recorded while participants were performing an interpersonal gambling game
with opponents’ facial emotions given as feedback. The results yielded that emotional
cues modulated the influence of monetary feedback on outcome valuation. Critically,
this modulation was more conspicuous in females: opponents’ angry expressions
increased females’ risky tendency and decreased the amplitude of reward positivity
(RewP) and feedback P300. These findings indicate that females are more sensitive
to emotional expressions in real interpersonal interactions, which is manifested in both
early motivational salience detection and late conscious cognitive appraisal stages of
feedback processing.
Keywords: gender difference, interpersonal emotion, decision making, RewP, feedback P300
INTRODUCTION
Females are believed to have superiority in emotional competence such as understanding other
people’s emotions embedded in facial cues (Hall, 1978; Hall and Matsumoto, 2004; Kret and De
Gelder, 2012; Sawada et al., 2014; Weisenbach et al., 2014), even among adolescents and infants
(McClure, 2000; Lee et al., 2013). However, it remains unclear whether this advantage extends to
real interpersonal interactions, as the participants in previous studies were required to recognize
emotions from static images without a naturalistic social-emotional context (Hall, 1978; Filkowski
et al., 2017). This is of great importance given that decoding of emotional information always takes
place in a specific context (Fukushima and Hiraki, 2006; Jack and Schyns, 2015; Wiggert et al.,
2015; Pádua Júnior et al., 2016). Therefore, the present study approached this issue by recording
behavioral and electrophysiological responses while participants performing an interpersonal
gambling game with opponents’ facial emotions given as feedback (Chen et al., 2017).
It is widely reported that females are more sensitive to facial emotions in comparison with males
(McClure, 2000; Donges et al., 2012; Erol et al., 2013; Lee et al., 2013; Weisenbach et al., 2014). For
instance, females were more accurate in the categorization of fearful expressions relative to males
in facial emotion perception test (Weisenbach et al., 2014) and females’ judgments of distance
were more likely to be influenced by facial emotions (Kim and Son, 2015). And such behavioral
advantage was also observed in adolescence, with girls more sensitive to facial emotions than boys
(Lee et al., 2013). This female superiority in emotion decoding was also observed at subliminal level.
1 July 2018 | Volume 12 | Article 275
Chen et al.
For example, in subliminal affective priming experiment, Donges
et al. (2012) reported that females manifested greater affective
priming due to happy faces than males did. Likewise, Hoffmann
et al. (2010) found that females were more accurate than males
in recognizing subtle facial displays of emotion. Moreover, such
female advantage in facial emotion recognition extends to other
materials like voice (Demenescu et al., 2014; Lambrecht et al.,
2014), point light displays (Alaerts et al., 2011), music (Hunter
et al., 2011) and multisensory emotion expressions (Collignon
et al., 2010).
Corresponding to the behavioral performance, the female
superiority in emotion decoding is associated with different
neural pathways and varied neurodynamics. A recent
meta-analysis study showed that the medial prefrontal cortex,
anterior cingulate cortex, frontal pole and the thalamus were
more recruited in men relative to women during emotion
perception, while women showed distinct activation in bilateral
amygdala, hippocampus and some regions of the dorsal midbrain
(Filkowski et al., 2017), suggesting that males tend to recruit
bilateral prefrontal regions involved in rational thinking and
cognitive control whereas females tend to recruit bilateral
amygdala involved in quick emotional evaluation (AlRyalat,
2017). Regarding neurodynamics, it was reported that females
yielded significantly larger P100 to fearful faces than males in
emotion discrimination task (Lee et al., 2017), and generated
longer latency and higher amplitude P450 component than
males when explicitly detecting happy and sad faces among
neutral faces (Orozco and Ehlers, 1998), suggesting that female
advantage in emotion processing emerges in the early stage
of low-level visual feature processing and the late stage of
indepth emotionality evaluation. Likewise, females (but not
males) yielded conspicuous N200 and P300 responses to
moderately negative pictures (Li et al., 2008; Yuan et al., 2009)
and demonstrated enhanced N200 when viewed unpleasant
stimuli (Lithari et al., 2010), implying that gender difference in
emotion decoding prevails in the initial perceptual coding and
the deliberative categorization of the emotional expressions.
Furthermore, Güntekin and Başar (2007) found that females
generated significantly larger occipital beta responses (15–24 Hz)
than males during the presentation of face expressions and
argued that beta synchronization might mediate the female
advantage in emotion processing.
The studies reviewed above revealed important insight into
the female superiority in emotion processing. However, to the
best of our knowledge, the influence of contextual factors on
emotion processing has largely been neglected, despite these
factors exert great impact on how observers ultimately discern
facial expressions (Barrett et al., 2011; Kring and Campellone,
2012). Therefore, we hope to shed light on this issue by using
the interpersonal version of Gehring and Willoughby’s gambling
task (Gehring and Willoughby, 2002; Chen et al., 2017), in which
participants chose between two monetary options and received
feedback orthogonally combined monetary cues and emotional
cues (Vrtička et al., 2014). Using this interpersonal paradigm, we
hope to probe into the female advantage in emotion processing
in naturalistic context concurrent with emotional and monetary
feedback.
Frontiers in Human Neuroscience | www.frontiersin.org
Female Advantage in Interpersonal Emotion Decoding
The neurophysiological studies of feedback processing
focused on two event related potential (ERP) components. One
is the frontocentral peaking component roughly 250–300 ms
after feedback, which is thought to reflect early evaluation
of performance feedback and action monitoring (Zhou et al.,
2010; Ullsperger et al., 2014; Proudfit, 2015; Sambrook and
Goslin, 2015). It was originally linked to negative feedback
and referred as feedback related negativity (FRN; Gehring
and Willoughby, 2002; Yeung et al., 2004), however, more
recent research has indicated that the FRN effect may rather
be driven by a reward positivity (RewP), which attenuates
a default frontocentral N2 component and which is present
for positive but not for negative outcomes (Proudfit, 2015;
Heydari and Holroyd, 2016). The other is feedback-related
P300, a positive deflection with parietal distribution occurring
between 300 ms and 600 ms after feedback. This positive
component, linking with a more elaborated and conscious
appraisal of the motivational significance of performance
feedback, was reported to be larger for positive feedback in
comparison with negative feedback (Yeung et al., 2004; Leng
and Zhou, 2010; Li et al., 2010; Ulrich and Hewig, 2014;
Mason et al., 2016; Zhao et al., 2016). Moreover, these two
components are sensitive to both monetary and emotional
feedback, as the previous study reported that emotional
and monetary reward elicited morphologically similar RewP
(Ethridge et al., 2017) and feedback-related P300 (Oumeziane
et al., 2017).
Given that emotion cues can bias decision-making (van Kleef
et al., 2004; Averbeck and Duchaine, 2009; Parkinson et al.,
2012; Chen et al., 2017), we predicted that emotional cues would
interact with monetary cues in feedback processing. Specifically,
opponents’ angry expressions should increase risky tendency and
decrease RewP and feedback-related P300 associated with wins
and losses, while happy expressions demonstrate the opposite
effect if interpersonal emotion exerts its influence through
affective reaction (van Kleef, 2009). Moreover, considering that
females outperform males in emotion decoding (Hall, 1978;
Hall and Matsumoto, 2004; Kret and De Gelder, 2012; Sawada
et al., 2014; Weisenbach et al., 2014) and females are believed
to be more interpersonally sensitive than men (Briton and Hall,
1995; Spence et al., 1975), we hypothesized the modulation of
interpersonal emotions was more conspicuous in females relative
to males.
MATERIALS AND METHODS
Participants
Fifty right-handed university students (25 females) were
recruited to participate in this experiment. All participants
reported normal auditory and normal or corrected-to-normal
visual acuity and were free of neurological or psychiatric
problems. Four participants (two females) were excluded from
analysis due to excessive EEG artifacts in the recordings. The
remaining participants showed no significant difference between
genders on age, personality and emotional intelligence (EI; see
Table 1 for illustration). This study was carried out in accordance
with the recommendations of the Declaration of Helsinki. The
2 July 2018 | Volume 12 | Article 275
Chen et al.
TABLE 1 | Age, personality and emotional intelligence∗ of the participants as a function of gender.
Male (n = 18)
Age 19.52 ± 1.13
Neuroticism 2.95 ± 0.49
Extraversion 3.27 ± 0.51
Openness 3.18 ± 0.58
Agreeableness 3.19 ± 1.21
Conscientiousness 3.34 ± 0.46
EI 3.71 ± 0.26
∗
Personality were assessed with shortened Chinese version of the Costa and McCrae NEO-FFI (Yang et al., 1999), while emotional intelligence (EI) were assessed with
ESI (Schutte et al., 1998).
protocol was approved by the the Ethical Committee of Shaanxi
Normal University. All subjects gave written informed consent in
accordance with the Declaration of Helsinki.
Procedure
Upon entry into the lab, the participant was introduced to
a confederate of the same gender who would perform as
opponent in a gambling game through a computer network.
They were told they would played as competitors, that is to
say, a loss for the participant means a win for his/her opponent
in the same amount, and vice versa. And then their facial
expressions (happy, angry and neutral) were recorded using a
Canon EOS 600D and used as feedback stimuli. Unbeknownst
to the participant, the facial expression of the confederate was
prerecorded and validated in advance. Immediately after giving
informed consent, participants were endowed with ¥40. They
were told the money was theirs to risk during the study and
asked to place it in their wallets. Participants were told that
additional rewards or punishments were given based on their
performances. The actual earnings for the each participant
ranged from ¥30 to ¥50.
Following our previous study (Chen et al., 2017), the
task in the present study was adapted from Gehring and
Willoughby gambling task (Gehring and Willoughby, 2002).
The key adaption was the interactivity (Chen et al., 2017)
and the feedback which orthogonally combined with monetary
and emotional cues (Vrtička et al., 2008, 2014; Chen et al.,
2017). Figure 1 shows a schematic diagram of a trial in this
task. Specifically, after a fixation period, the participants were
told that the computer would select performer and observer
for each round of gambling randomly. The person selected
as the performer would view numeral 10 or 50 (cents) and
make a choice by pressing the corresponding button as soon
as possible. After the choice presented for 300–1500 ms
randomly, the observer saw the monetary outcome and chose
one of his/her facial expressions to indicate his/her attitude:
while happiness means he/she is happy with the outcome,
anger means he/she is angry with the outcome, and neutral
expressions means no specific emotions. Then, the selected
facial expression overlaid with the monetary cues (‘‘+50’’ or
‘‘−50’’) on the forehead were presented as feedback for 1000 ms.
While ‘‘+’’ indicated that the performer won the points,
‘‘−’’ indicated the performer lose the points. Unbeknownst to
the participant, the monetary outcomes and affective responses
of the confederate were predetermined. Each participant was
Frontiers in Human Neuroscience | www.frontiersin.org
Female Advantage in Interpersonal Emotion Decoding
Female (n = 18) t P
19.08 ± 1.02 −1.42 0.16
2.68 ± 0.48 1.87 0.07
3.32 ± 0.40 −0.34 0.73
3.26 ± 0.68 −0.43 0.67
2.93 ± 0.61 0.52 0.61
3.37 ± 0.41 −0.25 0.80
3.83 ± 0.34 −1.39 0.17
FIGURE 1 | Schematic diagram of an experimental trial in the interpersonal
gambling task. After a fixation, the computer selected performer (red square)
and observer (green square) for each round of gambling randomly. The person
selected as the performer would view numeral 10 or 50 (cents) and make a
choice by pressing the corresponding button as soon as possible. After the
choice presented for 300–1500 ms randomly, the observer saw the monetary
outcome and chose one of his/her facial expressions to indicate his/her
attitude: happiness means he/she is happy with the outcome, anger means
he/she is angry with the outcome, neutral means no specific emotion. Then,
the selected facial expression overlaid with the monetary cues (“+50” or
“−50”) on the forehead were presented as feedback for 1000 ms. While “+”
means won, “−” means lose.
selected as performer two thirds of the trials and as observer the
remaining third. Each participant received four types of feedback
(happy-win, happy-lose, angry-win and angry-lose) equally with
64 trials. To make the game more realistic, 32 neutral-win
and 32 neutral-lose trials were included as fillers, which were
not included in the data analysis. The whole experiment
consisted of 448 trials, dividing into eight blocks with 56 trials
each.
EEG Recording
EEG measurements were recorded at 64 scalp sites using tin
electrodes mounted in an elastic cap (Brain Product, Munich,
Germany) according to the modified expanded 10–20 system,
each referenced online to FCZ. Vertical electrooculogram (EOG)
was recorded supra-orbitally and infra-orbitally from the right
eye. The horizontal EOG was recorded as the left vs. right orbital
rim. The EEG and EOG measurements were amplified using a
0.05–100 Hz bandpass and continuously digitized at 1000 Hz for
offline analysis. The impedance of all electrodes was kept less
than 5 kΩ.
3 July 2018 | Volume 12 | Article 275
Chen et al.
FIGURE 2 | Behavioral performance. (A) Mean rates of risky choice, (B) the corresponding reaction times (RTs) and (C) rates of emotional feedback selection as a
function of conditions for females and males separately. Error bars indicate standard error.
Data Analysis
Preprocessing
The ‘‘10’’ is defined as the low-risk option (small potential win
or loss) while the ‘‘50’’ is defined as the high-risk option (large
potential win or loss). The risk-seeking preference was measured
as the ‘‘risk ratio’’ by dividing the number of high-risk choices by
the total number of choices. Following previous studies (Gehring
and Willoughby, 2002; Chen et al., 2017), we analyzed the
preceding outcome on risky behavior in the current trial. Thus,
the risk ratio of the second trial during consecutive trials and
the corresponding reaction times (RTs; beyond three standard
deviations were excluded in RT calculation) were calculated as
the dependent variable (see Figure 2).
EEG data was preprocessed using EEGLAB (eeglab13_6_5b),
an open source toolbox running on the MATLAB platform
(R2014a). First, the data were high pass filtered at 0.5 Hz,
and re-referenced offline to bilateral mastoid electrodes. The
data were segmented into epochs around the presentation of
outcome feedback stimuli (−200 to 800 ms post stimulus).
The epoched data were baseline corrected using 200 ms before
the onset of the feedback. EEG epochs with large artifacts
(exceeding ±100 µV) were removed, and channels with poor
signal quality were interpolated spherically using EEGLAB
toolbox (Perrin et al., 1989). Trials contaminated by eye
blinks and other artifacts were corrected using an independent
component analysis algorithm (Delorme and Makeig, 2004).
There were on average 59.89 ± 4.17, 59.46 ± 3.71, 59.75 ± 4.48
and 59.21 ± 4.90 artifact-free trials obtained for the lose-
angry, lose-happy, win-angry and win-happy conditions for
females, while 58.83 ± 2.91, 58.61 ± 2.47, 57.56 ± 3.18 and
58.44 ± 3.27 remained for males. Note that the magnitude
Frontiers in Human Neuroscience | www.frontiersin.org
Female Advantage in Interpersonal Emotion Decoding
(10 vs. 50) of the outcome was collapsed for conciseness. After
low-pass filtered at 30 Hz, extracted average waveforms for
each participant and condition were used to calculate grand-
average waveforms. For statistical analyses, following previous
studies (Calvo and Beltrán, 2013; Chen et al., 2017), the
mean amplitude between 220 ms and 280 ms over fronto-
central cluster (F1, Fz, F2, FC1, FCz, FC2, C1, Cz, C2)
was calculated for RewP, whereas the mean activity between
300 ms and 500 ms at the parietal cluster (P1, Pz, P2,
PO3, POz, PO4) was calculated to assess feedback P300 (see
Figure 3).
Statistical Analysis
We entered the behavioral data and ERP data into repeated
measures ANOVAs, with the outcome valence (loss vs. win) and
emotion (happy vs. angry) as within-subject factors and gender
(male vs. female) as a between-subject factor. To examine how
participants take the current interpersonal gambling task, the
rates of each emotional expressions they chosen as feedback were
analyzed accordingly. The degrees of freedom of the F-ratio were
corrected per the Greenhouse–Geisser method, and multiple
comparisons were Bonferroni adjusted if necessary. The effect
sizes are shown as partial eta squared (ηp2 ).
RESULTS
Behavioral Performance
The participants selected more high-risk options after losses
(0.54 ± 0.02) than after wins (0.42 ± 0.03), (F (1,44) = 15.45,
p < 0.001, ηp2 = 0.26). Moreover, there were marginal
significant two-way interaction between emotion and outcome
4 July 2018 | Volume 12 | Article 275
Chen et al.
FIGURE 3 | Neurophysiological results. (A) Group-averaged event related potential (ERP) voltage waveforms over Cz, (B) scalp topography (top view shown) and (C)
bar plots of mean ERP values for reward positivity (RewP) and P300 during the selected time window as function of conditions. Error bars indicate standard error.
(F (1,44) = 3.29, p = 0.08, ηp2 = 0.06), and marginal significant
two-way interaction between emotion and gender (F (1,44) = 3.88,
p = 0.05, ηp2 = 0.08). Simple effect analysis indicated that the
difference in risky selection was more conspicuous following
opponents’ angry expressions (win: 0.43 ± 0.04 vs. lose:
0.56 ± 0.03, p < 0.001) in comparison with happy expressions
(win: 0.41 ± 0.04 vs. lose: 0.51 ± 0.03, p = 0.02; see
Figure 2A). Additionally, while females’ choices tended to be
affected by opponents’ expressions (happy: 0.45 ± 0.03 vs. angry:
0.48 ± 0.03, p = 0.05), males’ choices were immune to opponents’
expressions (happy: 0.50 ± 0.03 vs. angry: 0.49 ± 0.03,
p = 0.39). The analysis on RTs only showed a significant
main effect of emotion (F (1,44) = 5.29, p = 0.03, ηp2 = 0.11),
with the RTs longer following opponents happy expressions
(805 ± 22 ms) relative to angry expressions (788 ± 22 ms; see
Figure 2B).
The analysis on rates of emotional expression only
showed a two-way interaction between emotion and outcome
(F (2,88) = 10.11, p = 0.002, ηp2 = 0.19). Simple effect analysis
indicated that the angry expressions (0.21 ± 0.03) were less
selected than both happy (0.43 ± 0.03, p = 0.01) and neutral
(0.36 ± 0.04, p = 0.03) expressions if opponent lost the
game, in contrast, happy expressions (0.21 ± 0.03) were less
selected than both angry (0.42 ± 0.04, p = 0.01) and neutral
Frontiers in Human Neuroscience | www.frontiersin.org
Female Advantage in Interpersonal Emotion Decoding
(0.38 ± 0.04, p = 0.01) expressions if opponent won the game
(see Figure 2C).
Neurophysiological Performance
The analysis of RewP showed a main effect of emotion
(F (1,44) = 9.32, p = 0.004, ηp2 = 0.18), a significant interaction
of emotion × gender (F (1,44) = 4.42, p = 0.04, ηp2 = 0.09),
and a marginal significant interaction of emotion × outcome
valence (F (1,44) = 3.32, p = 0.07, ηp2 = 0.07). Simple effect
analysis (see Figure 3) indicated females differentiated the angry
(−0.32 ± 0.68 µV) from happy (0.69 ± 0.73 µV, p < 0.01)
expressions, while males failed to do this (angry: 0.63 ± 0.68 µV
vs. happy: 0.81 ± 0.73 µV, p = 0.53). Moreover, the RewP
was more positive going following happy expressions (0.84 ±
0.57 µV) relative to angry expressions (−0.09 ± 0.46 µV, p =
0.002) if participants won the game, whereas the RewP was hardly
differentiated between emotions (happy: 0.66 ± 0.49 µV vs.
angry: 0.40 ± 0.52 µV, p = 0.31) if participants lost the game.
The analysis of P300 amplitudes showed a main effect of
outcome valence (F (1,44) = 25.22, p < 0.001, ηp2 = 0.37), and a
main effect of emotion (F (1,44) = 7.77, p = 0.008, ηp2 = 0.15).
Also significant were the interaction of emotion × outcome
valence (F (1,44) = 12.98, p = 0.001, ηp2 = 0.23), and a significant
interaction of outcome valence × gender (F (1,44) = 4.63, p = 0.03,
5 July 2018 | Volume 12 | Article 275
Chen et al.
ηp2 = 0.10). Critically, the three-way interaction of emotion ×
outcome valence × gender is significant (F (1,44) = 4.94, p = 0.03,
ηp2 = 0.10). Simple effects analysis yielded that, for the females,
the wins (4.70 ± 0.46 µV) elicited larger P300 amplitudes than
the losses (3.86 ± 0.43 µV, p = 0.001) when accompanied with
happy expressions, while the P300 differences between wins
(4.32 ± 0.51 µV) and losses (4.43 ± 0.47 µV, p = 0.44) were
diminished when accompanied by angry expressions. In contrast,
for the males, the wins elicited larger P300 than losses when
accompanied by both angry (5.92 ± 0.51 µV vs. 5.17 ± 0.47 µV,
p < 0.001) and happy (5.58 ± 0.46 µV vs. 4.60 ± 0.42 µV, p <
0.001) expressions.
DISCUSSION
To examine the female superiority of emotion decoding
in a real social context, this study required participants
to play an interpersonal gambling game with monetary
and emotional cues orthogonally combined as feedback.
The results yielded that participants selected more happy
expressions for opponents’ losses but more angry expressions for
opponents’ wins. Moreover, participants selected more high-risk
options following losses relative to wins, and such effect was
more conspicuous when accompanied with opponents’ angry
expressions. Additionally, while females’ risky tendency was
affected by opponents’ emotional feedback, males showed no
such tendency. Corresponding to these behavioral results, RewP
and feedback P300 for females was influenced by opponents’
emotional feedback, but not for males. The significance of these
findings will be addressed as the following.
According to Emotions as Social Information Model (van
Kleef, 2009), emotional expressions affect observers’ behavior
by triggering inferential processes and/or affective reactions
in them, consequently, emotional expressions can be used as
strategy to influence observers’ behavior (Xiao and Houser,
2005). The participants in current study chose more happiness
for opponents’ losses but more anger for opponents’ wins,
indicating that they were aware of the setup of the experiment
and used emotional expressions as tactics to affect opponents.
In turn, we assumed that participants would take opponents’
emotional feedback seriously given that they performed
strategically when they had the right to give emotional feedback.
And thus, this result can evidence the good validity of our
interpersonal gambling game.
In line with previous studies (Gehring and Willoughby, 2002;
Yeung et al., 2004; Chen et al., 2017), participants were more
likely to gamble on risky outcomes if on the previous trial they
had lost the points. This might due to that participants were more
willing to anticipate larger monetary rewards in order to reduce
negative consequences. By contrast, they were more prone to
protect the money they had and thus showed more conservative
behavior when faced with rewarding feedback. Complement
to the previous studies, the current study showed that the
willingness to engage in risky choice following losses was affected
by opponents’ emotional feedback. Specifically, opponents’ angry
expressions enlarged the risky tendency relative to happy
expressions. Given that angry and happy expressions, used
Frontiers in Human Neuroscience | www.frontiersin.org
Female Advantage in Interpersonal Emotion Decoding
as social feedback, could bring in similar effect as monetary
feedback (Vrtička et al., 2014; Ethridge et al., 2017; Oumeziane
et al., 2017), we speculate that the current modification result
from the interaction of two types feedback cues. Moreover,
combined with the influence of emotional cues on RTs, the
current finding supported the assumption that interpersonal
emotions bias ones’ decision making (van Kleef et al., 2004;
Averbeck and Duchaine, 2009; Parkinson et al., 2012; Chen et al.,
2017).
Consistent with these behavioral findings, we observed
conspicuous interaction between monetary and emotional cues
on both the RewP and feedback P300. This finding replicated
the previous finding that opponent’s angry expressions reversed
the differentiation pattern of RewP/FRN and diminished
feedback P300 difference associated with losses and wins (Chen
et al., 2017). Following previous studies (Chen et al., 2017;
Proudfit, 2015; Heydari and Holroyd, 2016), we speculated
that this phenomenon might result from that opponents’ angry
expressions were taken as negative feedback and thus reduced the
positive-going deflection elicited by wins. Moreover, the current
finding was in accordance with the previous studies showing
that interpersonal emotional expressions affect negotiation
(van Kleef et al., 2004), dispute resolution (Friedman et al.,
2004), cooperation (Krumhuber et al., 2007), and prosocial
behaviors (van Doorn et al., 2015). Taken together, these
findings provided evidence for the assumption that emotional
information biases decision-making (Averbeck and Duchaine,
2009; Evans et al., 2011; Parkinson et al., 2012; Aïte et al.,
2013). Complement to the previous studies, the current findings
depicted the neurodynamics of the impact of interpersonal
emotions. Given that RewP/FRN is associated with early
evaluation of performance feedback and action monitoring
(Gehring and Willoughby, 2002; Holroyd et al., 2008; Ullsperger
et al., 2014; Proudfit, 2015) while P300 reflected elaborated
appraisal of the motivational significance of outcome (Yeung
et al., 2004; Leng and Zhou, 2010; Li et al., 2010; Ulrich
and Hewig, 2014; Mason et al., 2016; Zhao et al., 2016),
the current findings suggested that interpersonal emotions
might affect outcome processing during both early stage of
motivational salience monitoring and late stage of cognitive
appraisal processing.
More critical to the current study, we found that females were
more prone to be influenced by opponents’ emotional feedback.
That is, opponents’ angry expressions increased females’ risk
tendency, decreased RewP and feedback P300 in comparison
with happy expressions. Given that angry expressions have been
used as a negative social feedback (Vrtička et al., 2014; Ethridge
et al., 2017; Oumeziane et al., 2017) and elicited smaller RewP
(Ethridge et al., 2017) and feedback P300 (Oumeziane et al.,
2017), the current findings suggested that females are highly
susceptible to emotional feedback, and consquently modified the
amplitude of RewP and P300. Based on the modulation on RewP
and feedback P300, it seems the impact of angry expressions can
even overshadow the influence of monetary cues during both
early stage of motivational salience monitoring and late stage
of cognitive appraisal processing for females. In contrast, for
males, emotional feedback only counteracted effect of monetary
6 July 2018 | Volume 12 | Article 275
Chen et al.
cues during the early stage of salience monitoring, but not the
late stage of in-depth valuation. This finding was in accordance
with the neuroanatomical findings that while males tend to be
rational by recruiting bilateral prefrontal regions, females tend to
be emotional by recruiting bilateral amygdala when facing with
emotional information (AlRyalat, 2017; Filkowski et al., 2017).
Actually, females have long been believed to outperform males
at recognizing emotions expressions (McClure, 2000; Li et al.,
2008; Yuan et al., 2009; Donges et al., 2012; Erol et al., 2013;
Lee et al., 2013; Weisenbach et al., 2014; Mason et al., 2016),
and more prone to be influenced by emotional information
(Schirmer et al., 2002, 2004; Kim and Son, 2015). The current
conspicuous female advantage of emotion decoding during both
early stage of motivational salience monitoring (RewP) and
late stage of cognitive appraisal processing (feedback P300) was
in line with the findings that gender difference in emotions
processing emerges at early stage of emotion extraction (Lee et al.,
2017) and late stage of emotion in-depth processing (Orozco
and Ehlers, 1998). Taken together, the current study provided
convergent evidence for the gender difference in interpersonal
emotion decoding, adding new knowledge to this area by taking
the contextual factors into consideration (Barrett et al., 2011;
Kring and Campellone, 2012).
Although the explanation of the influence of angry expression
on feedback P300 is quite reasonable, the reverse of RewP/FRN
for losses and wins is still elusive. However, this phenomenon
seems to be robust, as we observed this pattern again (Chen
et al., 2017). One quite possible reason is the congruency between
emotional and monetary cues: the incongruence might result
in more negative valence. To support this speculation, a study
employed similar design reported that right inferior frontal gyrus
was more activated for incongruent feedback than for congruent
feedback (Vrtička et al., 2014). Another possible reason is that
emotional feedback is so salient that overshadow the influence
of monetary feedback. The big facial expressions overlaid with
small monetary cues in the current study might also boost
this tendency. However, all these speculations still need further
studies.
Despite the contributions of this study, some limitations
should be noted. First, the use of emotional expression taken
REFERENCES
Aïte, A., Borst, G., Moutier, S., Varescon, I., Brown, I., Houdé, O., et al. (2013).
Impact of emotional context congruency on decision making under ambiguity.
Emotion 13, 177–182. doi: 10.1037/a0031345
Alaerts, K., Nackaerts, E., Meyns, P., Swinnen, S. P., and Wenderoth, N. (2011).
Action and emotion recognition from point light displays: an investigation of
gender differences. PLoS One 6:e20989. doi: 10.1371/journal.pone.0020989
AlRyalat, S. A. (2017). Gender similarities and differences in brain activation
strategies: voxel-based meta-analysis on fMRI studies. J. Integr. Neurosci. 16,
227–240. doi: 10.3233/JIN-170015
Averbeck, B. B., and Duchaine, B. (2009). Integration of social and monetary
factors in decision making. Emotion 9, 599–608. doi: 10.1037/a0016509
Barrett, L. F., Mesquita, B., and Gendron, M. (2011). Context in emotion
perception. Curr. Dir. Psychol. Sci. 20, 286–290. doi: 10.1177/096372141
1422522
Bourne, V. J., and Maxwell, A. M. (2010). Examining the sex difference in
lateralisation for processing facial emotion: does biological sex or psychological
Frontiers in Human Neuroscience | www.frontiersin.org
Female Advantage in Interpersonal Emotion Decoding
from participants and confederates surely increase the ecological
validity, however, the external validity might be constrained.
Second, although we found conspicuous gender difference in
interpersonal emotion decoding after controlling age, personality
and EI, we did not take sex hormonal levels and menstrual cycle
into consideration. Given that sex hormones and cycle phases are
implicated in sexual dimorphism in facial emotion recognition
(Derntl et al., 2008; Guapo et al., 2009), future studies should
take these factors into consideration. Third, whether biological
sex or psychological gender identity matter in gender difference
(Bourne and Maxwell, 2010) in interpersonal emotion processing
is also an interesting topic in future studies.
CONCLUSION
The present study examined the gender difference in
interpersonal emotions processing. Participants were asked
to perform interpersonal gambling task with opponents’
emotional expressions presented as feedbacks. It was found that
opponents’ angry expressions increased females’ risky tendency
and decreased the amplitude of RewP and feedback P300. These
findings indicate that females are more sensitive to emotional
expressions in interpersonal interactions, which is manifested
during early stage of motivational salience monitoring and late
stage of conscious appraisal of outcomes.
AUTHOR CONTRIBUTIONS
XC, HY and TZ designed the study and discussed the results. HY,
TZ and YC organized the studies, analyzed the data and wrote a
first draft of the article, which was revised by YL.
FUNDING
This work was supported by Funded projects for the Academic
Leaders and Academic Backbones, Shaanxi Normal University
16QNGG006, Fundamental Research Funds for the Central
Universities under grant GK201603124, and Major project
of medicine science and technology of PLA (Grant no.
AWS17J012).
gender identity matter? Front. Hum. Neurosci. 48, 1289–1294. doi: 10.1016/j.
neuropsychologia.2009.12.032
Briton, N. J., and Hall, J. (1995). Gender-based expectancies and observer
judgments of smiling. J. Nonverbal. Behav. 19, 49–65. doi: 10.1007/bf02173412
Calvo, M. G., and Beltrán, D. (2013). Recognition advantage of happy faces: tracing
the neurocognitive processes. Neuropsychologia 51, 2051–2061. doi: 10.1016/j.
neuropsychologia.2013.07.010
Chen, X., Zheng, T., Han, L., Chang, Y., and Luo, Y. (2017). The neural dynamics
underlying the interpersonal effects of emotional expression on decision
making. Sci. Rep. 7:46651. doi: 10.1038/srep46651
Collignon, O., Girard, S., Gosselin, F., Saint-Amour, D., Lepore, F., and
Lassonde, M. (2010). Women process multisensory emotion expressions
more efficiently than men. Neuropsychologia 48, 220–225. doi: 10.1016/j.
neuropsychologia.2009.09.007
Delorme, A., and Makeig, S. (2004). EEGLAB: an open source toolbox for
analysis of single-trial EEG dynamics including independent component
analysis. J. Neurosci. Methods 134, 9–21. doi: 10.1016/j.jneumeth.2003.
10.009
7 July 2018 | Volume 12 | Article 275
Chen et al.
Demenescu, L. R., Mathiak, K. A., and Mathiak, K. (2014). Age- and gender-related
variations of emotion recognition in pseudowords and faces. Exp. Aging Res. 40,
187–207. doi: 10.1080/0361073X.2014.882210
Derntl, B., Kryspin-Exner, I., Fernbach, E., Moser, E., and Habel, U. (2008).
Emotion recognition accuracy in healthy young females is associated with cycle
phase. Horm. Behav. 53, 90–95. doi: 10.1016/j.yhbeh.2007.09.006
Donges, U. S., Kersting, A., and Suslow, T. (2012). Women’s greater ability to
perceive happy facial emotion automatically: gender differences in affective
priming. PLoS One 7:e41745. doi: 10.1371/journal.pone.0041745
Erol, A., Putgul, G., Kosger, F., and Ersoy, B. (2013). Facial emotion recognition
in schizophrenia: the impact of gender. Psychiatry Investig. 10, 69–74.
doi: 10.4306/pi.2013.10.1.69
Ethridge, P., Kujawa, A., Dirks, M. A., Arfer, K. B., Kessel, E. M., Klein, D. N., et al.
(2017). Neural responses to social and monetary reward in early adolescence
and emerging adulthood. Psychophysiology 54, 1786–1799. doi: 10.1111/psyp.
12957
Evans, S., Fleming, S. M., Dolan, R. J., and Averbeck, B. B. (2011). Effects
of emotional preferences on value-based decision-making are mediated by
mentalizing and not reward networks. J. Cogn. Neurosci. 23, 2197–2210.
doi: 10.1162/jocn.2010.21584
Filkowski, M. M., Olsen, R. M., Duda, B., Wanger, T. J., and Sabatinelli, D.
(2017). Sex differences in emotional perception: meta analysis of divergent
activation. Neuroimage 147, 925–933. doi: 10.1016/j.neuroimage.2016.
12.016
Friedman, R., Anderson, C., Brett, J., Olekalns, M., Goates, N., and Lisco, C. C.
(2004). The positive and negative effects of anger on dispute resolution:
evidence from electronically mediated disputes. J. Appl. Psychol. 89, 369–376.
doi: 10.1037/0021-9010.89.2.369
Fukushima, H., and Hiraki, K. (2006). Perceiving an opponent’s loss: gender-
related differences in the medial-frontal negativity. Soc. Cogn. Affect. Neurosci.
1, 149–157. doi: 10.1093/scan/nsl020
Gehring, W. J., and Willoughby, A. R. (2002). The medial frontal cortex and
the rapid processing of monetary gains and losses. Science 295, 2279–2282.
doi: 10.1126/science.1066893
Guapo, V. G., Graeff, F. G., Zani, A. C. T., Labate, C. M., dos Reis, R. M.,
and Del-Ben, C. M. (2009). Effects of sex hormonal levels and phases of the
menstrual cycle in the processing of emotional faces. Psychoneuroendocrinology
34, 1087–1094. doi: 10.1016/j.psyneuen.2009.02.007
Güntekin, B., and Başar, E. (2007). Gender differences influence brain’s β
oscillatory responses in recognition of facial expressions. Neurosci. Lett. 424,
94–99. doi: 10.1016/j.neulet.2007.07.052
Hall, J. A. (1978). Gender effects in decoding nonverbal cues. Psychol. Bull. 85,
845–857. doi: 10.1037/0033-2909.85.4.845
Hall, J. A., and Matsumoto, D. (2004). Gender differences in judgments of multiple
emotions from facial expressions. Emotion 4, 201–206. doi: 10.1037/1528-3542.
4.2.201
Heydari, S., and Holroyd, C. B. (2016). Reward positivity: reward prediction
error or salience prediction error? Curr. Behav. Neurosci. Rep. 53, 1185–1192.
doi: 10.1111/psyp.12673
Hoffmann, H., Kessler, H., Eppel, T., Rukavina, S., and Traue, H. C. (2010).
Expression intensity, gender and facial emotion recognition: women recognize
only subtle facial emotions better than men. Acta Psychol. 135, 278–283.
doi: 10.1016/j.actpsy.2010.07.012
Holroyd, C. B., Pakzad-Vaezi, K. L., and Krigolson, O. E. (2008). The feedback
correct-related positivity: sensitivity of the event-related brain potential to
unexpected positive feedback. Psychophysiology 45, 688–697. doi: 10.1111/j.
1469-8986.2008.00668.x
Hunter, P. G., Glenn Schellenberg, E., and Stalinski, S. M. (2011). Liking and
identifying emotionally expressive music: age and gender differences. J. Exp.
Child. Psychol. 110, 80–93. doi: 10.1016/j.jecp.2011.04.001
Jack, R. E., and Schyns, P. G. (2015). The human face as a dynamic tool for
social communication. Currt. Biol. 25, R621–R634. doi: 10.1016/j.cub.2015.
05.052
Kim, N.-G., and Son, H. (2015). How facial expressions of emotion affect distance
perception. Front. Psychol. 6:1825. doi: 10.3389/fpsyg.2015.01825
Kret, M. E., and De Gelder, B. (2012). A review on sex differences in
processing emotional signals. Neuropsychologia 50, 1211–1221. doi: 10.1016/j.
neuropsychologia.2011.12.022
Frontiers in Human Neuroscience | www.frontiersin.org
Female Advantage in Interpersonal Emotion Decoding
Kring, A. M., and Campellone, T. R. (2012). Emotion perception in schizophrenia:
context matters. Emot. Rev. 4, 182–186. doi: 10.1177/1754073911430140
Krumhuber, E., Manstead, A. S., Cosker, D., Marshall, D., Rosin, P. L., and
Kappas, A. (2007). Facial dynamics as indicators of trustworthiness and
cooperative behavior. Emotion 7, 730–735. doi: 10.1037/1528-3542.7.4.730
Lambrecht, L., Kreifelts, B., and Wildgruber, D. (2014). Gender differences in
emotion recognition: impact of sensory modality and emotional category.
Cogn. Emot. 28, 452–469. doi: 10.1080/02699931.2013.837378
Lee, S. A., Kim, C. Y., Shim, M., and Lee, S. H. (2017). Gender differences in neural
responses to perceptually invisible fearful face-an ERP study. Front. Behav.
Neurosci. 11:6. doi: 10.3389/fnbeh.2017.00006
Lee, N. C., Krabbendam, L., White, T. P., Meeter, M., Banaschewski, T.,
Barker, G. J., et al. (2013). Do you see what I see? Sex differences in the
discrimination of facial emotions during adolescence. Emotion 13, 1030–1040.
doi: 10.1037/a0033560
Leng, Y., and Zhou, X. (2010). Modulation of the brain activity in outcome
evaluation by interpersonal relationship: an ERP study. Neuropsychologia 48,
448–455. doi: 10.1016/j.neuropsychologia.2009.10.002
Li, P., Jia, S., Feng, T., Liu, Q., Suo, T., and Li, H. (2010). The influence of the
diffusion of responsibility effect on outcome evaluations: electrophysiological
evidence from an ERP study. Neuroimage 52, 1727–1733. doi: 10.1016/j.
neuroimage.2010.04.275
Li, H., Yuan, J., and Lin, C. (2008). The neural mechanism underlying the female
advantage in identifying negative emotions: an event-related potential study.
Neuroimage 40, 1921–1929. doi: 10.1016/j.neuroimage.2008.01.033
Lithari, C., Frantzidis, C. A., Papadelis, C., Vivas, A. B., Klados, M. A., Kourtidou-
Papadeli, C., et al. (2010). Are females more responsive to emotional stimuli? A
neurophysiological study across arousal and valence dimensions. Brain Topogr.
23, 27–40. doi: 10.1007/s10548-009-0130-5
Mason, L., Trujillo-Barreto, N. J., Bentall, R. P., and El-Deredy, W. (2016).
Attentional bias predicts increased reward salience and risk taking in bipolar
disorder. Biol. Psychiatry 79, 311–319. doi: 10.1016/j.biopsych.2015.03.014
McClure, E. B. (2000). A meta-analytic review of sex differences in facial
expression processing and their development in infants, children, and
adolescents. Psychol. Bull. 126, 424–453. doi: 10.1037/0033-2909.126.3.424
Orozco, S., and Ehlers, C. L. (1998). Gender differences in electrophysiological
responses to facial stimuli. Biol. Psychiatry 44, 281–289. doi: 10.1016/s0006-
3223(97)00487-3
Oumeziane, B. A., Schryer-Praga, J., and Foti, D. (2017). ‘‘Why don’t they
‘like’ me more?’’: comparing the time courses of social and monetary reward
processing. Neuropsychologia 107, 48–59. doi: 10.1016/j.neuropsychologia.
2017.11.001
Pádua Júnior, F. P., Prado, P. H. M., Roeder, S. S., and Andrade, E. B. (2016). What
a smile means: contextual beliefs and facial emotion expressions in a non-verbal
zero-sum game. Front. Psychol. 7:534. doi: 10.3389/fpsyg.2016.00534
Parkinson, B., Phiri, N., and Simons, G. (2012). Bursting with anxiety: adult social
referencing in an interpersonal Balloon Analogue Risk Task (BART). Emotion
12, 817–826. doi: 10.1037/a0026434
Perrin, F., Pernier, J., Bertrand, O., and Echallier, J. (1989). Spherical splines
for scalp potential and current density mapping. Electroencephalogr. Clin.
Neurophysiol. 72, 184–187. doi: 10.1016/0013-4694(89)90180-6
Proudfit, G. H. (2015). The reward positivity: from basic research on reward to
a biomarker for depression. Psychophysiology 52, 449–459. doi: 10.1111/psyp.
12370
Sambrook, T. D., and Goslin, J. (2015). A neural reward prediction error revealed
by a meta-analysis of ERPs using great grand averages. Psychol. Bull. 141,
213–235. doi: 10.1037/bul0000006
Sawada, R., Sato, W., Kochiyama, T., Uono, S., Kubota, Y., Yoshimura, S., et al.
(2014). Sex differences in the rapid detection of emotional facial expressions.
PLoS One 9:e94747. doi: 10.1371/journal.pone.0094747
Schirmer, A., Kotz, S. A., and Friederici, A. D. (2002). Sex differentiates the role
of emotional prosody during word processing. Cogn. Brain Res. 14, 228–233.
doi: 10.1016/s0926-6410(02)00108-8
Schirmer, A., Zysset, S., Kotz, S. A., and Yves von Cramon, D. (2004). Gender
differences in the activation of inferior frontal cortex during emotional speech
perception. Neuroimage 21, 1114–1123. doi: 10.1016/j.neuroimage.2003.10.048
Schutte, N. S., Malouff, J. M., Hall, L. E., Haggerty, D. J., Cooper, J. T.,
Golden, C. J., et al. (1998). Development and validation of a measure of
8 July 2018 | Volume 12 | Article 275
Chen et al.
emotional intelligence. Pers. Individ. Dif. 25, 167–177. doi: 10.1016/S0191-
8869(98)00001-4
Spence, J. T., Helmreich, R., and Stapp, J. (1975). Ratings of self and peers on sex
role attributes and their relation to self-esteem and conceptions of masculinity
and femininity. J. Pers. Soc. Psychol. 32, 29–39. doi: 10.1037/h0076857
Ullsperger, M., Fischer, A. G., Nigbur, R., and Endrass, T. (2014). Neural
mechanisms and temporal dynamics of performance monitoring. Trends.
Cogn. Sci. 18, 259–267. doi: 10.1016/j.tics.2014.02.009
Ulrich, N., and Hewig, J. (2014). A miss is as good as a mile? Processing of
near and full outcomes in a gambling paradigm. Psychophysiology 51, 819–823.
doi: 10.1111/psyp.12232
van Doorn, E. A., van Kleef, G. A., and van der Pligt, J. (2015). How emotional
expressions shape prosocial behavior: interpersonal effects of anger and
disappointment on compliance with requests. Motivat. Emot. 39, 128–141.
doi: 10.1007/s11031-014-9421-6
van Kleef, G. A. (2009). How emotions regulate social life: the emotions as
social information (EASI) model. Curr. Dir. in Psychol. Sci. 18, 184–188.
doi: 10.1111/j.1467-8721.2009.01633.x
van Kleef, G. A., De Dreu, C. K., and Manstead, A. S. (2004). The interpersonal
effects of anger and happiness in negotiations. J. Pers. Soc. Psychol. 86, 57–76.
doi: 10.1037/0022-3514.86.1.57
Vrtička, P., Andersson, F., Grandjean, D., Sander, D., and Vuilleumier, P.
(2008). Individual attachment style modulates human amygdala and striatum
activation during social appraisal. PLoS One 3:e2868. doi: 10.1371/journal.
pone.0002868
Vrtička, P., Sander, D., Anderson, B., Badoud, D., Eliez, S., and Debbané, M.
(2014). Social feedback processing from early to late adolescence: influence of
sex, age, and attachment style. Brain Behav. 4, 703–720. doi: 10.1002/brb3.251
Weisenbach, S. L., Rapport, L. J., Briceno, E. M., Haase, B. D., Vederman, A. C.,
Bieliauskas, L. A., et al. (2014). Reduced emotion processing efficiency in
healthy males relative to females. Soc. Cogn. Affect. Neurosci. 9, 316–325.
doi: 10.1093/scan/nss137
Wiggert, N., Wilhelm, F. H., Derntl, B., and Blechert, J. (2015). Gender differences
in experiential and facial reactivity to approval and disapproval during
Frontiers in Human Neuroscience | www.frontiersin.org
Female Advantage in Interpersonal Emotion Decoding
emotional social interactions. Front. Psychol. 6:1372. doi: 10.3389/fpsyg.2015.
01372
Xiao, E., and Houser, D. (2005). Emotion expression in human punishment
behavior. Proc. Natl. Acad. Sci. U S A 102, 7398–7401. doi: 10.1073/pnas.
0502399102
Yang, J., McCrae, R. R., Costa, P. T. Jr., Dai, X., Yao, S., Cai, T., et al. (1999). Cross-
cultural personality assessment in psychiatric populations: the NEO-PI—R in
the people’s republic of china. Psychol. Assess. 11, 359–368. doi: 10.1037/1040-
3590.11.3.359
Yeung, N., Botvinick, M. M., and Cohen, J. D. (2004). The neural basis of error
detection: conflict monitoring and the error-related negativity. Psychol. Rev.
111, 931–959. doi: 10.1037/0033-295x.111.4.939
Yuan, J. J., Luo, Y. J., Yan, J. H., Meng, X. X., Yu, F. Q., and Li, H. (2009). Neural
correlates of the females0 susceptibility to negative emotions: an insight into
gender-related prevalence of affective disturbances. Hum. Brain. Mapp. 30,
3676–3686. doi: 10.1002/hbm.20796
Zhao, D., Gu, R., Tang, P., Yang, Q., and Luo, Y. J. (2016). Incidental
emotions influence risk preference and outcome evaluation. Psychophysiology
53, 1542–1551. doi: 10.1111/psyp.12694
Zhou, Z., Yu, R., and Zhou, X. (2010). To do or not to do? Action enlarges the
FRN and P300 effects in outcome evaluation. Neuropsychologia 48, 3606–3613.
doi: 10.1016/j.neuropsychologia.2010.08.010
Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2018 Chen, Yuan, Zheng, Chang and Luo. This is an open-access article
distributed under the terms of the Creative Commons Attribution License (CC BY).
The use, distribution or reproduction in other forums is permitted, provided the
original author(s) and the copyright owner(s) are credited and that the original
publication in this journal is cited, in accordance with accepted academic practice.
No use, distribution or reproduction is permitted which does not comply with these
terms.
9 July 2018 | Volume 12 | Article 275